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Published in: Diabetology & Metabolic Syndrome 1/2018

Open Access 01-12-2018 | Research

Antioxidant effects of vitamins in type 2 diabetes: a meta-analysis of randomized controlled trials

Authors: Maria E. Balbi, Fernanda S. Tonin, Antonio M. Mendes, Helena H. Borba, Astrid Wiens, Fernando Fernandez-Llimos, Roberto Pontarolo

Published in: Diabetology & Metabolic Syndrome | Issue 1/2018

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Abstract

Background

Vitamins are essential micronutrients with antioxidant potential that may provide a complementary treatment for patients with chronic diseases. Our aim was to assess the effect of vitamin supplementation on the antioxidant status and glycemic index of type 2 diabetes mellitus patients.

Methods

We performed a systematic review with meta-analyses. Electronic searches were conducted in PubMed, Scopus, and Web of Science (December 2017). Randomized controlled trials evaluating the effect of any vitamin or vitamin complex supplementation on antioxidant status as primary outcome were included. The outcomes considered were: reduction of malondialdehyde (MDA); augmentation of glutathione peroxidase (GPx); changes in total antioxidant capacity (TAC), enhance in superoxide dismutase enzyme—SOD, and thiobarbituric acid reactive substances (TBARS). Outcomes of glycemic control were also evaluated. Pairwise meta-analyses were performed using software Review Manager 5.3.

Results

Thirty trials fulfilled the inclusion criteria, but only 12 could be included in the meta-analyses of antioxidant outcomes. The most commonly studied vitamins were B, C, D and E. Vitamin E was related to significant reduction of blood glucose as well as glycated hemoglobin compared to placebo, while both vitamins C and E were mainly associated with reducing MDA and TBARS and elevating GPx, SOD and TAC, compared to placebo. However, outcome reports in this field are still inconsistent (e.g. because of a lack of standard measures).

Conclusions

Supplementation of vitamin E may be a valuable strategy for controlling diabetes complications and enhancing antioxidant capacity. The effects of other micronutrients should be further investigated in larger and well-designed trials to properly place these complementary therapies in clinical practice.
Appendix
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Literature
1.
go back to reference American Diabetes Association. Standards of medical care in diabetes—2018. Diabetes Care. 2018;41(Suppl 1):S1–2. American Diabetes Association. Standards of medical care in diabetes—2018. Diabetes Care. 2018;41(Suppl 1):S1–2.
2.
go back to reference International Diabetes Federation. IDF diabetes atlas. 8th ed. Brussels: IDF; 2017. International Diabetes Federation. IDF diabetes atlas. 8th ed. Brussels: IDF; 2017.
3.
go back to reference Cobitz AR, Ambery P. Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care. 2009;32(5):e58.CrossRefPubMed Cobitz AR, Ambery P. Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care. 2009;32(5):e58.CrossRefPubMed
4.
go back to reference Johansen JS, Harris AK, Rychly DJ, Ergul A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc Diabetol. 2005;4:5.CrossRefPubMedPubMedCentral Johansen JS, Harris AK, Rychly DJ, Ergul A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc Diabetol. 2005;4:5.CrossRefPubMedPubMedCentral
5.
go back to reference Ceriello A, Testa R, Genovese S. Clinical implications of oxidative stress and potential role of natural antioxidants in diabetic vascular complications. Nutr Metab Cardiovasc Dis. 2016;26(4):285–92.CrossRefPubMed Ceriello A, Testa R, Genovese S. Clinical implications of oxidative stress and potential role of natural antioxidants in diabetic vascular complications. Nutr Metab Cardiovasc Dis. 2016;26(4):285–92.CrossRefPubMed
6.
go back to reference Manna P, Jain SK. Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: causes and therapeutic strategies. Metab Syndr Relat Disord. 2015;13(10):423–44.CrossRefPubMedPubMedCentral Manna P, Jain SK. Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: causes and therapeutic strategies. Metab Syndr Relat Disord. 2015;13(10):423–44.CrossRefPubMedPubMedCentral
7.
go back to reference Sankhla M, Sharma TK, Mathur K, Rathor JS, Butolia V, Gadhok AK, et al. Relationship of oxidative stress with obesity and its role in obesity induced metabolic syndrome. Clin Lab. 2012;58(5–6):385–92.PubMed Sankhla M, Sharma TK, Mathur K, Rathor JS, Butolia V, Gadhok AK, et al. Relationship of oxidative stress with obesity and its role in obesity induced metabolic syndrome. Clin Lab. 2012;58(5–6):385–92.PubMed
8.
go back to reference Kositsawat J, Freeman VL. Vitamin C and A1c relationship in the National Health and Nutrition Examination Survey (NHANES) 2003–2006. J Am Coll Nutr. 2011;30(6):477–83.CrossRefPubMed Kositsawat J, Freeman VL. Vitamin C and A1c relationship in the National Health and Nutrition Examination Survey (NHANES) 2003–2006. J Am Coll Nutr. 2011;30(6):477–83.CrossRefPubMed
9.
go back to reference Calles-Escandon J, Cipolla M. Diabetes and endothelial dysfunction: a clinical perspective. Endocr Rev. 2001;22(1):36–52.CrossRefPubMed Calles-Escandon J, Cipolla M. Diabetes and endothelial dysfunction: a clinical perspective. Endocr Rev. 2001;22(1):36–52.CrossRefPubMed
10.
go back to reference Hink U, Tsilimingas N, Wendt M, Munzel T. Mechanisms underlying endothelial dysfunction in diabetes mellitus: therapeutic implications. Treat Endocrinol. 2003;2(5):293–304.CrossRefPubMed Hink U, Tsilimingas N, Wendt M, Munzel T. Mechanisms underlying endothelial dysfunction in diabetes mellitus: therapeutic implications. Treat Endocrinol. 2003;2(5):293–304.CrossRefPubMed
11.
12.
13.
go back to reference Lamb RE, Goldstein BJ. Modulating an oxidative-inflammatory cascade: potential new treatment strategy for improving glucose metabolism, insulin resistance, and vascular function. Int J Clin Pract. 2008;62(7):1087–95.CrossRefPubMedPubMedCentral Lamb RE, Goldstein BJ. Modulating an oxidative-inflammatory cascade: potential new treatment strategy for improving glucose metabolism, insulin resistance, and vascular function. Int J Clin Pract. 2008;62(7):1087–95.CrossRefPubMedPubMedCentral
14.
go back to reference Mark SD, Wang W, Fraumeni JF Jr., Li JY, Taylor PR, Wang GQ, et al. Lowered risks of hypertension and cerebrovascular disease after vitamin/mineral supplementation: the Linxian Nutrition Intervention Trial. Am J Epidemiol. 1996;143(7):658–64.CrossRefPubMed Mark SD, Wang W, Fraumeni JF Jr., Li JY, Taylor PR, Wang GQ, et al. Lowered risks of hypertension and cerebrovascular disease after vitamin/mineral supplementation: the Linxian Nutrition Intervention Trial. Am J Epidemiol. 1996;143(7):658–64.CrossRefPubMed
15.
go back to reference White PA, Oliveira RC, Oliveira AP, Serafini MR, Araujo AA, Gelain DP, et al. Antioxidant activity and mechanisms of action of natural compounds isolated from lichens: a systematic review. Molecules. 2014;19(9):14496–527.CrossRefPubMed White PA, Oliveira RC, Oliveira AP, Serafini MR, Araujo AA, Gelain DP, et al. Antioxidant activity and mechanisms of action of natural compounds isolated from lichens: a systematic review. Molecules. 2014;19(9):14496–527.CrossRefPubMed
16.
go back to reference Singh R, Devi S, Gollen R. Role of free radical in atherosclerosis, diabetes and dyslipidaemia: larger-than-life. Diabetes Metab Res Rev. 2015;31(2):113–26.CrossRefPubMed Singh R, Devi S, Gollen R. Role of free radical in atherosclerosis, diabetes and dyslipidaemia: larger-than-life. Diabetes Metab Res Rev. 2015;31(2):113–26.CrossRefPubMed
17.
go back to reference Tabatabaei-Malazy O, Nikfar S, Larijani B, Abdollahi M. Influence of ascorbic acid supplementation on type 2 diabetes mellitus in observational and randomized controlled trials; a systematic review with meta-analysis. J Pharm Pharm Sci. 2014;17(4):554–82.CrossRefPubMed Tabatabaei-Malazy O, Nikfar S, Larijani B, Abdollahi M. Influence of ascorbic acid supplementation on type 2 diabetes mellitus in observational and randomized controlled trials; a systematic review with meta-analysis. J Pharm Pharm Sci. 2014;17(4):554–82.CrossRefPubMed
18.
go back to reference Montero D, Walther G, Stehouwer CD, Houben AJ, Beckman JA, Vinet A. Effect of antioxidant vitamin supplementation on endothelial function in type 2 diabetes mellitus: a systematic review and meta-analysis of randomized controlled trials. Obes Rev. 2014;15(2):107–16.CrossRefPubMed Montero D, Walther G, Stehouwer CD, Houben AJ, Beckman JA, Vinet A. Effect of antioxidant vitamin supplementation on endothelial function in type 2 diabetes mellitus: a systematic review and meta-analysis of randomized controlled trials. Obes Rev. 2014;15(2):107–16.CrossRefPubMed
19.
go back to reference Sarmento RA, Silva FM, Sbruzzi G, Schaan BD, Almeida JC. Antioxidant micronutrients and cardiovascular risk in patients with diabetes: a systematic review. Arq Bras Cardiol. 2013;101(3):240–8.PubMedPubMedCentral Sarmento RA, Silva FM, Sbruzzi G, Schaan BD, Almeida JC. Antioxidant micronutrients and cardiovascular risk in patients with diabetes: a systematic review. Arq Bras Cardiol. 2013;101(3):240–8.PubMedPubMedCentral
20.
go back to reference George PS, Pearson ER, Witham MD. Effect of vitamin D supplementation on glycaemic control and insulin resistance: a systematic review and meta-analysis. Diabet Med. 2012;29(8):e142–50.CrossRefPubMed George PS, Pearson ER, Witham MD. Effect of vitamin D supplementation on glycaemic control and insulin resistance: a systematic review and meta-analysis. Diabet Med. 2012;29(8):e142–50.CrossRefPubMed
21.
go back to reference Xu R, Zhang S, Tao A, Chen G, Zhang M. Influence of vitamin E supplementation on glycaemic control: a meta-analysis of randomised controlled trials. PLoS ONE. 2014;9(4):e95008.CrossRefPubMedPubMedCentral Xu R, Zhang S, Tao A, Chen G, Zhang M. Influence of vitamin E supplementation on glycaemic control: a meta-analysis of randomised controlled trials. PLoS ONE. 2014;9(4):e95008.CrossRefPubMedPubMedCentral
22.
go back to reference Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0: Cochrane. London: The cochrane collaboration; 2011. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0: Cochrane. London: The cochrane collaboration; 2011.
23.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG. The PRISMA Group. Preferred reporting items for systematic reviews and meta analyses: the PRISMA statement. J Clin Epidemiol. 2009;62:1006–12.CrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG. The PRISMA Group. Preferred reporting items for systematic reviews and meta analyses: the PRISMA statement. J Clin Epidemiol. 2009;62:1006–12.CrossRefPubMed
24.
go back to reference Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17(1):1–12.CrossRefPubMed Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17(1):1–12.CrossRefPubMed
25.
go back to reference Aghamohammadi V, Gargari BP, Aliasgharzadeh A. Effect of folic acid supplementation on homocysteine, serum total antioxidant capacity, and malondialdehyde in patients with type 2 diabetes mellitus. J Am Coll Nutr. 2011;30(3):210–5.CrossRefPubMed Aghamohammadi V, Gargari BP, Aliasgharzadeh A. Effect of folic acid supplementation on homocysteine, serum total antioxidant capacity, and malondialdehyde in patients with type 2 diabetes mellitus. J Am Coll Nutr. 2011;30(3):210–5.CrossRefPubMed
26.
go back to reference Anderson RA, Evans LM, Ellis GR, Khan N, Morris K, Jackson SK, et al. Prolonged deterioration of endothelial dysfunction in response to postprandial lipaemia is attenuated by vitamin C in type 2 diabetes. Diabet Med. 2006;23(3):258–64.CrossRefPubMed Anderson RA, Evans LM, Ellis GR, Khan N, Morris K, Jackson SK, et al. Prolonged deterioration of endothelial dysfunction in response to postprandial lipaemia is attenuated by vitamin C in type 2 diabetes. Diabet Med. 2006;23(3):258–64.CrossRefPubMed
27.
go back to reference Antoniades C, Tousoulis D, Tountas C, Tentolouris C, Toutouza M, Vasiliadou C, et al. Vascular endothelium and inflammatory process, in patients with combined Type 2 diabetes mellitus and coronary atherosclerosis: the effects of vitamin C. Diabet Med. 2004;21(6):552–8.CrossRefPubMed Antoniades C, Tousoulis D, Tountas C, Tentolouris C, Toutouza M, Vasiliadou C, et al. Vascular endothelium and inflammatory process, in patients with combined Type 2 diabetes mellitus and coronary atherosclerosis: the effects of vitamin C. Diabet Med. 2004;21(6):552–8.CrossRefPubMed
28.
go back to reference Ble-Castillo JL, Carmona-Diaz E, Mendez JD, Larios-Medina FJ, Medina-Santillan R, Cleva-Villanueva G, et al. Effect of alpha-tocopherol on the metabolic control and oxidative stress in female type 2 diabetics. Biomed Pharmacother. 2005;59(6):290–5.CrossRefPubMed Ble-Castillo JL, Carmona-Diaz E, Mendez JD, Larios-Medina FJ, Medina-Santillan R, Cleva-Villanueva G, et al. Effect of alpha-tocopherol on the metabolic control and oxidative stress in female type 2 diabetics. Biomed Pharmacother. 2005;59(6):290–5.CrossRefPubMed
29.
go back to reference Chen H, Karne RJ, Hall G, Campia U, Panza JA, Cannon RO 3rd, et al. High-dose oral vitamin C partially replenishes vitamin C levels in patients with Type 2 diabetes and low vitamin C levels but does not improve endothelial dysfunction or insulin resistance. Am J Physiol Heart Circ Physiol. 2006;290(1):H137–45.CrossRefPubMed Chen H, Karne RJ, Hall G, Campia U, Panza JA, Cannon RO 3rd, et al. High-dose oral vitamin C partially replenishes vitamin C levels in patients with Type 2 diabetes and low vitamin C levels but does not improve endothelial dysfunction or insulin resistance. Am J Physiol Heart Circ Physiol. 2006;290(1):H137–45.CrossRefPubMed
30.
go back to reference Dalan R, Liew H, Assam PN, Chan ES, Siddiqui FJ, Tan AW, et al. A randomised controlled trial evaluating the impact of targeted vitamin D supplementation on endothelial function in type 2 diabetes mellitus: the DIMENSION trial. Diabetes Vasc Dis Res. 2016;13(3):192–200.CrossRef Dalan R, Liew H, Assam PN, Chan ES, Siddiqui FJ, Tan AW, et al. A randomised controlled trial evaluating the impact of targeted vitamin D supplementation on endothelial function in type 2 diabetes mellitus: the DIMENSION trial. Diabetes Vasc Dis Res. 2016;13(3):192–200.CrossRef
31.
go back to reference Gariballa S, Afandi B, Abu Haltem M, Yassin J, Alessa A. Effect of antioxidants and B-group vitamins on risk of infections in patients with type 2 diabetes mellitus. Nutrients. 2013;5(3):711–24.CrossRefPubMedPubMedCentral Gariballa S, Afandi B, Abu Haltem M, Yassin J, Alessa A. Effect of antioxidants and B-group vitamins on risk of infections in patients with type 2 diabetes mellitus. Nutrients. 2013;5(3):711–24.CrossRefPubMedPubMedCentral
32.
go back to reference Haghighat NVM, Eghtesadi S, Heidari I, Hosseini A, Rostami A. The Effects of tocotrienols added to canola oil on microalbuminuria, inflammation, and nitrosative stress in patients with type 2 diabetes: a randomized, double-blind, placebo-controlled trial. Int J Prev Med. 2014;5(5):617–23.PubMedPubMedCentral Haghighat NVM, Eghtesadi S, Heidari I, Hosseini A, Rostami A. The Effects of tocotrienols added to canola oil on microalbuminuria, inflammation, and nitrosative stress in patients with type 2 diabetes: a randomized, double-blind, placebo-controlled trial. Int J Prev Med. 2014;5(5):617–23.PubMedPubMedCentral
33.
go back to reference Hejazi N, Dabbaghmanesh M, Mazloom Z, Dashtabi A. Effects of vitamin E on fasting and postprandial oxidative stress, inflammatory markers, glucose status, insulin resistance, blood pressure and pulse rate in type-2 diabetic patients: a randomized clinical trial. Galen Med J. 2015;4(3):67–74. Hejazi N, Dabbaghmanesh M, Mazloom Z, Dashtabi A. Effects of vitamin E on fasting and postprandial oxidative stress, inflammatory markers, glucose status, insulin resistance, blood pressure and pulse rate in type-2 diabetic patients: a randomized clinical trial. Galen Med J. 2015;4(3):67–74.
34.
go back to reference Jamalan M, Rezazadeh M, Zeinali M, Ghaffari MA. Effect of ascorbic acid and alpha-tocopherol supplementations on serum leptin, tumor necrosis factor alpha, and serum amyloid A levels in individuals with type 2 diabetes mellitus. Avicenna J Phytomed. 2015;5(6):531–9.PubMedPubMedCentral Jamalan M, Rezazadeh M, Zeinali M, Ghaffari MA. Effect of ascorbic acid and alpha-tocopherol supplementations on serum leptin, tumor necrosis factor alpha, and serum amyloid A levels in individuals with type 2 diabetes mellitus. Avicenna J Phytomed. 2015;5(6):531–9.PubMedPubMedCentral
35.
go back to reference Jorde R, Figenschau Y. Supplementation with cholecalciferol does not improve glycaemic control in diabetic subjects with normal serum 25-hydroxyvitamin D levels. Eur J Nutr. 2009;48(6):349–54.CrossRefPubMed Jorde R, Figenschau Y. Supplementation with cholecalciferol does not improve glycaemic control in diabetic subjects with normal serum 25-hydroxyvitamin D levels. Eur J Nutr. 2009;48(6):349–54.CrossRefPubMed
36.
go back to reference Lai MH. Antioxidant effects and insulin resistance improvement of chromium combined with vitamin C and e supplementation for type 2 diabetes mellitus. J Clin Biochem Nutr. 2008;43(3):191–8.CrossRefPubMedPubMedCentral Lai MH. Antioxidant effects and insulin resistance improvement of chromium combined with vitamin C and e supplementation for type 2 diabetes mellitus. J Clin Biochem Nutr. 2008;43(3):191–8.CrossRefPubMedPubMedCentral
37.
go back to reference Lu Q, Bjorkhem I, Wretlind B, Diczfalusy U, Henriksson P, Freyschuss A. Effect of ascorbic acid on microcirculation in patients with type II diabetes: a randomized placebo-controlled cross-over study. Clin Sci. 2005;108(6):507–13.CrossRefPubMed Lu Q, Bjorkhem I, Wretlind B, Diczfalusy U, Henriksson P, Freyschuss A. Effect of ascorbic acid on microcirculation in patients with type II diabetes: a randomized placebo-controlled cross-over study. Clin Sci. 2005;108(6):507–13.CrossRefPubMed
38.
go back to reference Mahmoudabadi MM, Rahbar AR. Effect of EPA and vitamin C on superoxide dismutase, glutathione peroxidase, total antioxidant capacity and malondialdehyde in type 2 diabetic patients. Oman Med J. 2014;29(1):39–45.CrossRefPubMedPubMedCentral Mahmoudabadi MM, Rahbar AR. Effect of EPA and vitamin C on superoxide dismutase, glutathione peroxidase, total antioxidant capacity and malondialdehyde in type 2 diabetic patients. Oman Med J. 2014;29(1):39–45.CrossRefPubMedPubMedCentral
39.
go back to reference Manzella D, Barbieri M, Ragno E, Paolisso G. Chronic administration of pharmacologic doses of vitamin E improves the cardiac autonomic nervous system in patients with type 2 diabetes. Am J Clin Nutr. 2001;73(6):1052–7.CrossRefPubMed Manzella D, Barbieri M, Ragno E, Paolisso G. Chronic administration of pharmacologic doses of vitamin E improves the cardiac autonomic nervous system in patients with type 2 diabetes. Am J Clin Nutr. 2001;73(6):1052–7.CrossRefPubMed
40.
go back to reference Mason SA, Della Gatta PA, Snow RJ, Russell AP, Wadley GD. Ascorbic acid supplementation improves skeletal muscle oxidative stress and insulin sensitivity in people with type 2 diabetes: findings of a randomized controlled study. Free Radic Biol Med. 2016;93:227–38.CrossRefPubMed Mason SA, Della Gatta PA, Snow RJ, Russell AP, Wadley GD. Ascorbic acid supplementation improves skeletal muscle oxidative stress and insulin sensitivity in people with type 2 diabetes: findings of a randomized controlled study. Free Radic Biol Med. 2016;93:227–38.CrossRefPubMed
41.
go back to reference Mazloom ZHN, Dabbaghmanesh MH, Tabatabaei HR, Ahmadi A, Ansar H. Effect of vitamin C supplementation on postprandial oxidative stress and lipid profile in type 2 diabetic patients. Pak J Biol Sci. 2011;14(19):900–4.CrossRefPubMed Mazloom ZHN, Dabbaghmanesh MH, Tabatabaei HR, Ahmadi A, Ansar H. Effect of vitamin C supplementation on postprandial oxidative stress and lipid profile in type 2 diabetic patients. Pak J Biol Sci. 2011;14(19):900–4.CrossRefPubMed
42.
go back to reference Mullan BA, Young IS, Fee H, McCance DR. Ascorbic acid reduces blood pressure and arterial stiffness in type 2 diabetes. Hypertension. 2002;40(6):804–9.CrossRefPubMed Mullan BA, Young IS, Fee H, McCance DR. Ascorbic acid reduces blood pressure and arterial stiffness in type 2 diabetes. Hypertension. 2002;40(6):804–9.CrossRefPubMed
43.
go back to reference Nikooyeh B, Neyestani TR, Farvid M, Alavi-Majd H, Houshiarrad A, Kalayi A, et al. Daily consumption of vitamin D − or vitamin D + calcium-fortified yogurt drink improved glycemic control in patients with type 2 diabetes: a randomized clinical trial. Am J Clin Nutr. 2011;93(4):764–71.CrossRefPubMed Nikooyeh B, Neyestani TR, Farvid M, Alavi-Majd H, Houshiarrad A, Kalayi A, et al. Daily consumption of vitamin D − or vitamin D + calcium-fortified yogurt drink improved glycemic control in patients with type 2 diabetes: a randomized clinical trial. Am J Clin Nutr. 2011;93(4):764–71.CrossRefPubMed
44.
go back to reference Nikooyeh B, Neyestani TR, Tayebinejad N, Alavi-Majd H, Shariatzadeh N, Kalayi A, et al. Daily intake of vitamin D −  or calcium-vitamin D-fortified Persian yogurt drink (doogh) attenuates diabetes-induced oxidative stress: evidence for antioxidative properties of vitamin D. J Hum Nutr Diet. 2014;27(Suppl 2):276–83.CrossRefPubMed Nikooyeh B, Neyestani TR, Tayebinejad N, Alavi-Majd H, Shariatzadeh N, Kalayi A, et al. Daily intake of vitamin D −  or calcium-vitamin D-fortified Persian yogurt drink (doogh) attenuates diabetes-induced oxidative stress: evidence for antioxidative properties of vitamin D. J Hum Nutr Diet. 2014;27(Suppl 2):276–83.CrossRefPubMed
45.
go back to reference Paolisso G, Tagliamonte MR, Barbieri M, Zito GA, Gambardella A, Varricchio G, et al. Chronic vitamin E administration improves brachial reactivity and increases intracellular magnesium concentration in type II diabetic patients. J Clin Endocrinol Metab. 2000;85(1):109–15.CrossRefPubMed Paolisso G, Tagliamonte MR, Barbieri M, Zito GA, Gambardella A, Varricchio G, et al. Chronic vitamin E administration improves brachial reactivity and increases intracellular magnesium concentration in type II diabetic patients. J Clin Endocrinol Metab. 2000;85(1):109–15.CrossRefPubMed
46.
go back to reference Park S, Choi SB. Effects of alpha-tocopherol supplementation and continuous subcutaneous insulin infusion on oxidative stress in Korean patients with type 2 diabetes. Am J Clin Nutr. 2002;75(4):728–33.CrossRefPubMed Park S, Choi SB. Effects of alpha-tocopherol supplementation and continuous subcutaneous insulin infusion on oxidative stress in Korean patients with type 2 diabetes. Am J Clin Nutr. 2002;75(4):728–33.CrossRefPubMed
47.
go back to reference Reaven PD, Herold DA, Barnett J, Edelman S. Effects of Vitamin E on susceptibility of low-density lipoprotein and low-density lipoprotein subfractions to oxidation and on protein glycation in NIDDM. Diabetes Care. 1995;18(6):807–16.CrossRefPubMed Reaven PD, Herold DA, Barnett J, Edelman S. Effects of Vitamin E on susceptibility of low-density lipoprotein and low-density lipoprotein subfractions to oxidation and on protein glycation in NIDDM. Diabetes Care. 1995;18(6):807–16.CrossRefPubMed
48.
go back to reference Shab-Bidar SNTR, Djazayery A. The interactive effect of improvement of vitamin D status and VDR FokI variants on oxidative stress in type 2 diabetic subjects: a randomized controlled trial. Eur J Clin Nutr. 2015;69(2):216–22.CrossRefPubMed Shab-Bidar SNTR, Djazayery A. The interactive effect of improvement of vitamin D status and VDR FokI variants on oxidative stress in type 2 diabetic subjects: a randomized controlled trial. Eur J Clin Nutr. 2015;69(2):216–22.CrossRefPubMed
49.
go back to reference Sugden JA, Davies JI, Witham MD, Morris AD, Struthers AD. Vitamin D improves endothelial function in patients with Type 2 diabetes mellitus and low vitamin D levels. Diabet Med. 2008;25(3):320–5.CrossRefPubMed Sugden JA, Davies JI, Witham MD, Morris AD, Struthers AD. Vitamin D improves endothelial function in patients with Type 2 diabetes mellitus and low vitamin D levels. Diabet Med. 2008;25(3):320–5.CrossRefPubMed
50.
go back to reference Tessier DM, Khalil A, Trottier L, Fulop T. Effects of vitamin C supplementation on antioxidants and lipid peroxidation markers in elderly subjects with type 2 diabetes. Arch Gerontol Geriatr. 2009;48(1):67–72.CrossRefPubMed Tessier DM, Khalil A, Trottier L, Fulop T. Effects of vitamin C supplementation on antioxidants and lipid peroxidation markers in elderly subjects with type 2 diabetes. Arch Gerontol Geriatr. 2009;48(1):67–72.CrossRefPubMed
51.
go back to reference Vafa MHN, Moslehi N, Eghtesadi S, Heydari I. Effect of tocotrienols enriched canola oil on glycemic control and oxidative status in patients with type 2 diabetes mellitus: a randomized double-blind placebo-controlled clinical trial. J Res Med Sci. 2015;20(6):540–7.CrossRefPubMedPubMedCentral Vafa MHN, Moslehi N, Eghtesadi S, Heydari I. Effect of tocotrienols enriched canola oil on glycemic control and oxidative status in patients with type 2 diabetes mellitus: a randomized double-blind placebo-controlled clinical trial. J Res Med Sci. 2015;20(6):540–7.CrossRefPubMedPubMedCentral
52.
go back to reference Winterbone MS, Sampson MJ, Saha S, Hughes JC, Hughes DA. Pro-oxidant effect of alpha-tocopherol in patients with type 2 diabetes after an oral glucose tolerance test—a randomised controlled trial. Cardiovasc Diabetol. 2007;6:8.CrossRefPubMedPubMedCentral Winterbone MS, Sampson MJ, Saha S, Hughes JC, Hughes DA. Pro-oxidant effect of alpha-tocopherol in patients with type 2 diabetes after an oral glucose tolerance test—a randomised controlled trial. Cardiovasc Diabetol. 2007;6:8.CrossRefPubMedPubMedCentral
53.
go back to reference Witham MD, Dove FJ, Dryburgh M, Sugden JA, Morris AD, Struthers AD. The effect of different doses of vitamin D(3) on markers of vascular health in patients with type 2 diabetes: a randomised controlled trial. Diabetologia. 2010;53(10):2112–9.CrossRefPubMed Witham MD, Dove FJ, Dryburgh M, Sugden JA, Morris AD, Struthers AD. The effect of different doses of vitamin D(3) on markers of vascular health in patients with type 2 diabetes: a randomised controlled trial. Diabetologia. 2010;53(10):2112–9.CrossRefPubMed
54.
go back to reference Wu JH, Ward NC, Indrawan AP, Almeida CA, Hodgson JM, Proudfoot JM, et al. Effects of alpha-tocopherol and mixed tocopherol supplementation on markers of oxidative stress and inflammation in type 2 diabetes. Clin Chem. 2007;53(3):511–9.CrossRefPubMed Wu JH, Ward NC, Indrawan AP, Almeida CA, Hodgson JM, Proudfoot JM, et al. Effects of alpha-tocopherol and mixed tocopherol supplementation on markers of oxidative stress and inflammation in type 2 diabetes. Clin Chem. 2007;53(3):511–9.CrossRefPubMed
55.
go back to reference Yiu YF, Yiu KH, Siu CW, Chan YH, Li SW, Wong LY, et al. Randomized controlled trial of vitamin D supplement on endothelial function in patients with type 2 diabetes. Atherosclerosis. 2013;227(1):140–6.CrossRefPubMed Yiu YF, Yiu KH, Siu CW, Chan YH, Li SW, Wong LY, et al. Randomized controlled trial of vitamin D supplement on endothelial function in patients with type 2 diabetes. Atherosclerosis. 2013;227(1):140–6.CrossRefPubMed
56.
go back to reference Ashor AW, Siervo M, Lara J, Oggioni C, Afshar S, Mathers JC. Effect of vitamin C and vitamin E supplementation on endothelial function: a systematic review and meta-analysis of randomised controlled trials. Br J Nutr. 2015;113(8):1182–94.CrossRefPubMed Ashor AW, Siervo M, Lara J, Oggioni C, Afshar S, Mathers JC. Effect of vitamin C and vitamin E supplementation on endothelial function: a systematic review and meta-analysis of randomised controlled trials. Br J Nutr. 2015;113(8):1182–94.CrossRefPubMed
57.
go back to reference Brigelius-Flohe R, Kelly FJ, Salonen JT, Neuzil J, Zingg JM, Azzi A. The European perspective on vitamin E: current knowledge and future research. Am J Clin Nutr. 2002;76(4):703–16.CrossRefPubMed Brigelius-Flohe R, Kelly FJ, Salonen JT, Neuzil J, Zingg JM, Azzi A. The European perspective on vitamin E: current knowledge and future research. Am J Clin Nutr. 2002;76(4):703–16.CrossRefPubMed
58.
go back to reference Mahreen R, Mohsin M, Nasreen Z, Siraj M, Ishaq M. Significantly increased levels of serum malondialdehyde in type 2 diabetics with myocardial infarction. Int J Diabetes Dev Ctries. 2010;30(1):49–51.CrossRefPubMedPubMedCentral Mahreen R, Mohsin M, Nasreen Z, Siraj M, Ishaq M. Significantly increased levels of serum malondialdehyde in type 2 diabetics with myocardial infarction. Int J Diabetes Dev Ctries. 2010;30(1):49–51.CrossRefPubMedPubMedCentral
59.
go back to reference Rani AJ, Mythili SV. Study on total antioxidant status in relation to oxidative stress in type 2 diabetes mellitus. J Clin Diagn Res. 2014;8(3):108–10.PubMedPubMedCentral Rani AJ, Mythili SV. Study on total antioxidant status in relation to oxidative stress in type 2 diabetes mellitus. J Clin Diagn Res. 2014;8(3):108–10.PubMedPubMedCentral
60.
go back to reference Fenercioglu AK, Saler T, Genc E, Sabuncu H, Altuntas Y. The effects of polyphenol-containing antioxidants on oxidative stress and lipid peroxidation in Type 2 diabetes mellitus without complications. J Endocrinol Invest. 2010;33(2):118–24.CrossRefPubMed Fenercioglu AK, Saler T, Genc E, Sabuncu H, Altuntas Y. The effects of polyphenol-containing antioxidants on oxidative stress and lipid peroxidation in Type 2 diabetes mellitus without complications. J Endocrinol Invest. 2010;33(2):118–24.CrossRefPubMed
61.
go back to reference Khodaeian M, Tabatabaei-Malazy O, Qorbani M, Farzadfar F, Amini P, Larijani B. Effect of vitamins C and E on insulin resistance in diabetes: a meta-analysis study. Eur J Clin Invest. 2015;45(11):1161–74.CrossRefPubMed Khodaeian M, Tabatabaei-Malazy O, Qorbani M, Farzadfar F, Amini P, Larijani B. Effect of vitamins C and E on insulin resistance in diabetes: a meta-analysis study. Eur J Clin Invest. 2015;45(11):1161–74.CrossRefPubMed
62.
go back to reference Rafighi ZSA, Arab S, Mohd Yousof R. Association of dietary vitamin C and e intake and antioxidant enzymes in type 2 diabetes mellitus patients. Glob J Health Sci. 2013;5(3):183–7.CrossRefPubMedPubMedCentral Rafighi ZSA, Arab S, Mohd Yousof R. Association of dietary vitamin C and e intake and antioxidant enzymes in type 2 diabetes mellitus patients. Glob J Health Sci. 2013;5(3):183–7.CrossRefPubMedPubMedCentral
63.
go back to reference Church TS, Earnest CP, Wood KA, Kampert JB. Reduction of C-reactive protein levels through use of a multivitamin. Am J Med. 2003;115(9):702–7.CrossRefPubMed Church TS, Earnest CP, Wood KA, Kampert JB. Reduction of C-reactive protein levels through use of a multivitamin. Am J Med. 2003;115(9):702–7.CrossRefPubMed
64.
go back to reference Gey KF, Moser UK, Jordan P, Stahelin HB, Eichholzer M, Ludin E. Increased risk of cardiovascular disease at suboptimal plasma concentrations of essential antioxidants: an epidemiological update with special attention to carotene and vitamin C. Am J Clin Nutr. 1993;57(5 Suppl):787S–97S.CrossRefPubMed Gey KF, Moser UK, Jordan P, Stahelin HB, Eichholzer M, Ludin E. Increased risk of cardiovascular disease at suboptimal plasma concentrations of essential antioxidants: an epidemiological update with special attention to carotene and vitamin C. Am J Clin Nutr. 1993;57(5 Suppl):787S–97S.CrossRefPubMed
65.
go back to reference Gey KF, Puska P, Jordan P, Moser UK. Inverse correlation between plasma vitamin E and mortality from ischemic heart disease in cross-cultural epidemiology. Am J Clin Nutr. 1991;53(1 Suppl):326S–34S.CrossRefPubMed Gey KF, Puska P, Jordan P, Moser UK. Inverse correlation between plasma vitamin E and mortality from ischemic heart disease in cross-cultural epidemiology. Am J Clin Nutr. 1991;53(1 Suppl):326S–34S.CrossRefPubMed
66.
go back to reference Pittas AG, Lau J, Hu FB, Dawson-Hughes B. The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J Clin Endocrinol Metab. 2007;92(6):2017–29.CrossRefPubMedPubMedCentral Pittas AG, Lau J, Hu FB, Dawson-Hughes B. The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J Clin Endocrinol Metab. 2007;92(6):2017–29.CrossRefPubMedPubMedCentral
67.
go back to reference Mokhtari Z, Hekmatdoost A, Nourian M. Antioxidant efficacy of vitamin D. J Parathyr Dis. 2017;5(1):11–6. Mokhtari Z, Hekmatdoost A, Nourian M. Antioxidant efficacy of vitamin D. J Parathyr Dis. 2017;5(1):11–6.
68.
go back to reference Lindstrom J, Ilanne-Parikka P, Peltonen M, Aunola S, Eriksson JG, Hemio K, et al. Sustained reduction in the incidence of type 2 diabetes by lifestyle intervention: follow-up of the Finnish Diabetes Prevention Study. Lancet. 2006;368(9548):1673–9.CrossRefPubMed Lindstrom J, Ilanne-Parikka P, Peltonen M, Aunola S, Eriksson JG, Hemio K, et al. Sustained reduction in the incidence of type 2 diabetes by lifestyle intervention: follow-up of the Finnish Diabetes Prevention Study. Lancet. 2006;368(9548):1673–9.CrossRefPubMed
69.
go back to reference Krul-Poel YH, Ter Wee M, Lips P, Simsek S. Management of endocrine disease: The effect of vitamin D supplementation on glycaemic control in patients with Type 2 Diabetes Mellitus: a systematic review and meta-analysis. Eur J Endocrinol. 2017;176(1):R1–14.CrossRefPubMed Krul-Poel YH, Ter Wee M, Lips P, Simsek S. Management of endocrine disease: The effect of vitamin D supplementation on glycaemic control in patients with Type 2 Diabetes Mellitus: a systematic review and meta-analysis. Eur J Endocrinol. 2017;176(1):R1–14.CrossRefPubMed
70.
go back to reference Beveridge LA, Struthers AD, Khan F, Jorde R, Scragg R, Macdonald HM, et al. Effect of vitamin D supplementation on blood pressure: a systematic review and meta-analysis incorporating individual patient data. JAMA Intern Med. 2015;175(5):745–54.CrossRefPubMed Beveridge LA, Struthers AD, Khan F, Jorde R, Scragg R, Macdonald HM, et al. Effect of vitamin D supplementation on blood pressure: a systematic review and meta-analysis incorporating individual patient data. JAMA Intern Med. 2015;175(5):745–54.CrossRefPubMed
71.
go back to reference Liu RH. Dietary bioactive compounds and their health implications. J Food Sci. 2013;78(Suppl 1):A18–25.CrossRefPubMed Liu RH. Dietary bioactive compounds and their health implications. J Food Sci. 2013;78(Suppl 1):A18–25.CrossRefPubMed
72.
go back to reference Huang D, Ou B, Prior RL. The chemistry behind antioxidant capacity assays. J Agric Food Chem. 2005;53(6):1841–56.CrossRefPubMed Huang D, Ou B, Prior RL. The chemistry behind antioxidant capacity assays. J Agric Food Chem. 2005;53(6):1841–56.CrossRefPubMed
73.
go back to reference Jones CW, Keil LG, Holland WC, Caughey MC, Platts-Mills TF. Comparison of registered and published outcomes in randomized controlled trials: a systematic review. BMC Med. 2015;13:282.CrossRefPubMedPubMedCentral Jones CW, Keil LG, Holland WC, Caughey MC, Platts-Mills TF. Comparison of registered and published outcomes in randomized controlled trials: a systematic review. BMC Med. 2015;13:282.CrossRefPubMedPubMedCentral
Metadata
Title
Antioxidant effects of vitamins in type 2 diabetes: a meta-analysis of randomized controlled trials
Authors
Maria E. Balbi
Fernanda S. Tonin
Antonio M. Mendes
Helena H. Borba
Astrid Wiens
Fernando Fernandez-Llimos
Roberto Pontarolo
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2018
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/s13098-018-0318-5

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